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On August 2, 1943, Kennedy's boat, PT-109, along with PT-162 and PT-169, were ordered to continue nighttime patrol near New Georgia in the Solomon Islands, when it was rammed by the Japanese destroyer Amagiri. Kennedy gathered his surviving crew members together in the water around the wreckage, to vote on whether to "fight or surrender". Kennedy stated, "There's nothing in the book about a situation like this. A lot of you men have families and some of you have children. What do you want to do? I have nothing to lose." Shunning surrender, the men swam towards a small island. Kennedy, despite re-injury to his back in the collision, towed a badly burned crewman through the water with a life jacket strap clenched between his teeth. He towed the wounded man to the island and later to a second island from where his crew was subsequently rescued. For these actions, Kennedy received the Navy and Marine Corps Medal with the following citation: For extremely heroic conduct as Commanding Officer of Motor Torpedo Boat 109 following the collision and sinking of that vessel in the Pacific War Theater on August 1--2, 1943. Unmindful of personal danger, Lieutenant (then Lieutenant, Junior Grade) Kennedy unhesitatingly braved the difficulties and hazards of darkness to direct rescue operations, swimming many hours to secure aid and food after he had succeeded in getting his crew ashore. His outstanding courage, endurance and leadership contributed to the saving of several lives and were in keeping with the highest traditions of the United States Naval Service.

In October 1943, Kennedy took command of a PT boat converted into a gun boat, PT-59, which in November took part in a Marine rescue on Choiseul Island. Kennedy was honorably discharged in early 1945, just prior to Japan's surrender. Kennedy's other decorations in World War II included the Purple Heart, American Defense Service Medal, American Campaign Medal, Asiatic-Pacific Campaign Medal with three bronze service stars, and the World War II Victory Medal. When later asked by a reporter how he became a war hero, Kennedy joked: "It was involuntary. They sank my boat."

While Kennedy was still serving, his older brother Joseph P. Kennedy, Jr. was killed in action on August 12, 1944 while part of Operation Aphrodite. Since Joe Jr. had been the family's political standard-bearer, the task now fell on John.

In 1946, U.S. Representative James Michael Curley vacated his seat in the strong Democratic 10th Congressional district in Massachusetts to become mayor of Boston. Kennedy ran for the seat, beating his Republican opponent by a large margin; this, despite not having previously included politics in his career planning. He was a congressman for six years but had a mixed voting record, often diverging from President Harry S. Truman and the rest of the Democratic Party.

In 1952, he defeated incumbent Republican Henry Cabot Lodge, Jr. for the U.S. Senate. The following year he was married to wife Jacqueline.

Kennedy underwent several spinal operations over the following two years, was at times critically ill and received Catholic last rites, and was often absent from the Senate. During his convalescence in 1956, he published Profiles in Courage, a book about U.S. Senators who risked their careers for their personal beliefs, and which received the Pulitzer Prize for Biography in 1957. Rumors that this work was co-authored by his close adviser and speechwriter, Ted Sorensen, were confirmed in Sorensen's 2008 autobiography.